Tropical Medicine and

Infectious Disease

Article
An Innovative Public–Private Mix Model for
Improving Tuberculosis Care in Vietnam: How Well
Are We Doing?
Thuong Do Thu 1, *, Ajay M. V. Kumar 2,3,4 , Gomathi Ramaswamy 5 , Thurain Htun 6 ,
Hoi Le Van 1 , Luan Nguyen Quang Vo 7 , Thuy Thi Thu Dong 7 , Andrew Codlin 7 ,
Rachel Forse 7 , Jacob Crewsell 8 , Hoi Nguyen Thanh 9 , Hai Nguyen Viet 1 , Huy Bui Van 1 ,
Hoa Nguyen Binh 1,3,10 and Nhung Nguyen Viet 1,10
1 Vietnam Integrated Center for Tuberculosis and Respirology Research, Vietnam National Lung Hospital,
Vietnam Tuberculosis Control Programme, Hanoi 100000, Vietnam; hoilv@yahoo.com (H.L.V.);
nguyenviethai.hmu@gmail.com (H.N.V.); vhcapri@gmail.com (H.B.V.);
nguyenbinhhoatb@yahoo.com (H.N.B.); VietNhung@yahoo.com (N.N.V.)
2 International Union Against Tuberculosis and Lung Disease, South-East Asia Office, New Delhi 110016,
India; akumar@theunion.org
3 International Union Against Tuberculosis and Lung Disease, Paris 75006, France
4 Yenepoya Medical College, Yenepoya (Deemed to be University), Mangaluru 575018, India
5 National Centre of Excellence and Advanced Research on Anemia Control, Centre for Community Medicine,
All India Institute of Medical Sciences, New Delhi 110029, India; gmthramaswamy@gmail.com
6 International Union Against Tuberculosis and Lung Disease, Mandalay 05021, Myanmar;
thurainhtun30111990@gmail.com
7 Friends for International Tuberculosis Relief, Ho Chi Minh City 700000, Vietnam;
luan.vo@tbhelp.org (L.N.Q.V.); thuy.dong@tbhelp.org (T.T.T.D.); Andrew.codlin@tbhelp.org (A.C.);
rachel.forse@tbhelp.org (R.F.)
8 Stop TB Partnership, Geneva 1218, Switzerland; jacobc@stoptb.org
9 Haiphong International General Hospital, Haiphong 180000, Vietnam; hoinguyenthanhbm@gmail.com
10 Hanoi Medical University, Hanoi 100000, Vietnam
* Correspondence: thuthuong0308@gmail.com; Tel.: +84-343007914 (ext. 235); Fax: +84-438326162




Received: 14 November 2019; Accepted: 10 February 2020; Published: 14 February 2020


Abstract: To improve tuberculosis (TB) care among individuals attending a private tertiary care
hospital in Vietnam, an innovative private sector engagement model was implemented from June
to December 2018. This included: (i) Active facility-based screening of all adults for TB symptoms
(and chest x-ray (CXR) for those with symptoms) by trained and incentivized providers, with on-site
diagnostic testing or transport of sputum samples, (ii) a mobile application to reduce dropout in the
care cascade and (iii) enhanced follow-up care by community health workers. We conducted a cohort
study using project and routine surveillance data for evaluation. Among 52,078 attendees, 368 (0.7%)
had symptoms suggestive of TB and abnormalities on CXR. Among them, 299 (81%) were tested and
103 (34.4%) were diagnosed with TB. In addition, 195 individuals with normal CXR were indicated
for TB testing by attending clinicians, of whom, seven were diagnosed with TB. Of the 110 TB patients
diagnosed, 104 (95%) were initiated on treatment and 97 (93%) had a successful treatment outcome.
Given the success of this model, the National TB Programme is considering to scale it up nationwide
after undertaking a detailed cost-effectiveness analysis.

Keywords: public–private mix model; public–private partnership; missing cases; operational research;
SORT IT

Trop. Med. Infect. Dis. 2020, 5, 26; doi:10.3390/tropicalmed5010026 www.mdpi.com/journal/tropicalmed

Trop. Med. Infect. Dis. 2020, 5, 26 2 of 13

1. Introduction
Tuberculosis (TB) is the leading cause of mortality from a single infectious agent globally,
accounting for 1.45 million deaths annually [1]. The global community has pledged to end the TB
epidemic by 2030 [2]. While there has been progress, the rate of decline of TB incidence has been
modest at ~2% each year [3]. At this rate, we will not be able to realize the goal of ending TB by 2030.
To accelerate progress, the Stop TB Partnership recommends that countries should strive to achieve
90-(90)-90 targets (diagnosing 90% of all people with TB including 90% among key populations and
treating 90% of them successfully) [4].
One of the major challenges in TB control is “missing cases”. Globally, of the 10 million people
estimated to have developed TB in 2018, only 7 million were notified [1]. The gap of 3 million includes
people who are not diagnosed and treated, and those managed in the private health sector, but not
notified to National Tuberculosis Programmes (NTP).
A multi-country study found that in more than 60% of TB patients, the private sector was the first
point of contact, yet the proportion of cases notified to NTP was less than 10% [5]. Also, health care
provision in the private sector is not standardized and poorly regulated in many countries. These may
lead to delays in diagnosis and treatment, improper case management, increased risk of developing
drug resistance, disease transmission, and catastrophic health expenditure [6]. Engagement and
collaboration with private sector in those countries where a large proportion of care seeking is sought
with private providers in critical [2].
Vietnam is one among the 30 high TB burden countries and has strong private health care sector.
It is estimated that approximately 50% of TB patients seek initial care in the private sector before
visiting the public health system [7,8]. In 2018, only 57% of estimated incident cases were notified to
NTP, meaning there is no information about the rest of the patients and a majority of these may be
receiving care in the private sector [1]. Mirroring the global picture, previous studies from Vietnam
have also reported mismanagement in diagnosis and treatment of TB in the private health sector [9–11].
All these findings underline the need to engage the private health care providers in Vietnam’s TB care
and prevention efforts.
To engage the private sector, several public–private mix (PPM) models have been implemented by
the Vietnam NTP since 2001. One such model involved training of private health care providers and
strengthening referral mechanisms between the private sector and NTP. This yielded an increase in
overall TB case detection rate of Ho Chi Minh City by 7% [12], but there were several gaps. About 30%
of presumptive TB patients referred to NTP for sputum microscopy did not reach the diagnostic facility
and nearly 60% of the patients diagnosed were lost to follow-up before starting treatment. Of those
started on treatment, only 60% successfully completed it [13].
To address these gaps, a new model was implemented in Haiphong International General Hospital
(HIGH) in 2018 as part of the TB REACH-funded Zero TB Vietnam initiative. This model included
three unique components: (i) active facility-based screening of all adults for TB symptoms (and chest
x-ray (CXR) for those with symptoms) by trained and incentivized providers, with on-site diagnostic
testing or transport of sputum samples, (ii) an innovative mobile application to reduce dropout in the
care cascade and iii) enhanced follow-up care through engagement of a local network of community
health workers (CHWs). However, this model has not yet been systematically evaluated. In this
study, we aimed to evaluate the performance of this private sector engagement model by tracking
the cascade of tuberculosis care among the individuals attending the HIGH in Vietnam from June to
December 2018.The specific objectives were to determine, (i) the number (proportion) with presumptive
tuberculosis and among them, the number (proportion) who were investigated for tuberculosis (ii)
the number (proportion) diagnosed with tuberculosis and initiated on treatment (iii) the treatment
outcomes among those initiated on treatment and (iv) the delays involved at different steps of the
care cascade.
Trop. Med. Infect. Dis. 2020, 5, 26 3 of 13

2. Materials and Methods

2.1. Study Design

This was a cohort study involving analysis of routine surveillance data.

2.2. Setting
Vietnam is a South-East Asian country with a population of 93.7 million. The country is divided
into 63 provinces, which are further divided into districts, communes, and sub-communes. About 34.4%
of the population live in urban areas and about 10% people are below the poverty line [14]. Healthcare
services are provided by both public and private sectors.

2.2.1. TB Control Program in Vietnam

The public health facilities for TB care and prevention are managed either directly by the NTP
or indirectly through the Department of Health (DOH). Under the NTP, TB diagnosis, treatment,
and control activities are carried out by the national level unit, 63 TB and lung disease hospitals or
provincial TB units, and 707 TB management units (TBMUs) at the district level.

2.2.2. PPM Models

There has been significant progress in the implementation of PPM initiatives for TB care and
prevention in Vietnam. There are four types of PPM models. PPM Model 1 entails the referral of
presumptive TB patients identified by the private providers to NTP for further evaluation. PPM Model
2 encompasses the diagnosis of TB and referral to the NTP. PPM Model 3 entails the provision of
directly-observed treatment. PPM model 4 provides both diagnostic and treatment services similar to
a TBMU. Private providers participating in PPM initiatives are trained for TB screening, diagnosis with
sputum smear microscopy, and recording and reporting as per NTP guidelines.

2.2.3. PPM Model at HIGH

PPM model at HIGH is similar to the model 4. HIGH was chosen for the intervention because it is
the biggest tertiary care private hospital in Haiphong province (considered a poor-performing province
by NTP) and there was political commitment from the director of the HIGH to collaborate with the NTP.
Three departments from the HIGH (Endocrinology, Otolaryngology, and Respiratory medicine) were
targeted for systematic screening. These three departments were chosen because they were expected to
account for the majority of pulmonary presumptive TB patients visiting HIGH. The doctors and nurses
of these departments were trained on the management of TB cases as per NTP guidelines and were
given incentives for TB screening, diagnosis and treatment, and systematic recording and reporting.
A total of 110 USD of fixed allowance per month was provided to the hospital. About 70 USD was
provided every month for conducting the monthly review meetings and printing of forms. In addition,
performance-based incentives were provided: (i) 0.5 USD given to the nurse for each chest X-ray
conducted (ii) 1 USD given to the nurse for each sample transported for Xpert MTB/RIF testing (iii)
2 USD given to the doctor for each patient diagnosed with TB (iv) 3 USD given to the doctor for
each TB patient completing treatment. The project was supervised by a focal point (@45 USD per
month), PPM coordinator (@130 USD per month) and a PPM supervisor (@130 USD per month).
These incentives were on top of the salaries they received. Thus, the total cost incurred on the project
for six months was 4100 USD. All costs were incurred in Viet Nam Dong and translated to USD based
on the average exchange rate during the implementation period.
All out-patients attending the selected departments (Endocrinology, Otolaryngology,
and Respiratory medicine) were screened for symptoms such as cough, hemoptysis, chest pain
and dyspnea, fever, fatigue and unexpected weight loss. Individuals who had any of these symptoms
or who had a history of contact with TB were requested to undergo chest radiography. Contacts were
Trop. Med. Infect. Dis. 2020, 5, 26 4 of 13

defined as people living in the same household with a TB patient for at least two nights per week
during the last 6 months. Individuals with symptoms suggestive of TB or exposure to a person with TB
and parenchymal abnormalities suggestive of TB on chest X-ray were considered ‘presumptive TB’ and
evaluated further for bacteriologic confirmation. The chest radiographs of the presumptive TB patients
were examined by the radiologists at HIGH. Patients with TB symptoms and no abnormalities on chest
X-ray were also offered tests for bacteriological confirmation based on the discretion of the attending
physician. Spot sputum samples (without induction) were collected from the patients. For those who
were not able to produce sputum, bronchoscopy was suggested by the treating physician and the
bronchial washings were used for further testing. Patients with lymphadenopathy were referred for
histopathological examination for confirmation of TB.
Individuals with a positive symptom screen were counselled by the treating physician about the
different diagnostic tests available and their costs and were offered one of more of the following tests
in the hospital for bacteriological confirmation: (i) Transcription Concerted Reaction (TRC) Ready 80
test (ii) sputum microscopy (iii) liquid culture and drug susceptibility test for first-line drugs. The TRC
Ready 80 test is an automated molecular assay designed to detect mycobacterium tuberculosis (MTB)
complex 16S rRNA present in clinical specimens (pulmonary and extra-pulmonary) or culture isolates.
This has been described in greater detail elsewhere [15]. Though this test not endorsed by the WHO
yet, it has been approved for use in Vietnam by the MOH for diagnosing TB. Chest X-ray screening
and diagnostic tests at HIGH were paid by the patient at the following rates: 3 USD for chest X-ray,
3 USD for microscopy, 12 USD for culture, and 36 USD for TRC Ready 80. For patients unable to afford
these tests, sputum samples were collected and transported to a nearby NTP facility for TB diagnosis
using Xpert MTB/RIF assay, which was offered free of charge. The nurses in HIGH were trained on the
procedures of sputum collection in falcon tubes, packaging and transportation in cold chain to the
nearby NTP facility (which is located at a distance of 1.5 kms from HIGH). Nurses transported the
sputum specimens in-person at the end of the day to the NTP facility.
Patients diagnosed with TB disease either through bacteriologic confirmation or clinical diagnosis
were initiated on anti-TB treatment at an NTP facility or a private health facility of the patient’s
choice. Patients diagnosed with drug-susceptible TB were treated with first-line drugs and those
with rifampicin resistance were referred to the NTP’s provincial TB hospital for further evaluation.
While drugs were provided free of charge to the patients at NTP facilities, patients paid out of pocket
at private health facilities.
The CHWs were notified immediately after the diagnosis of each TB patient for linkage to care
and follow-up from treatment start until completion. CHWs were motivated volunteers identified
from each commune and recruited to support TB care and prevention activities in the Zero TB project
(under funding support of TB REACH grant). They were mostly women and received formal training
(for two days by NTP staff) on screening, counselling, follow-up care and support of TB patients. In the
community, CHWs performed household contact tracing and counseling on treatment adherence and
infection control. They received performance-based incentives as part of another project and did not
receive any specific incentives for the project described in this study. The study’s case definitions and
treatment outcomes were in accordance with NTP and WHO guidelines.

2.2.4. Recording and Reporting

All patient details were entered in the ACIS (Access to Care Information System, Clinton Health
Access Initiative/TechUp, Vietnam) application, a data collection and case management tool for
persons with presumptive TB in the community. Dedicated tablets with preinstalled software were
procured and provided to the nurses and were trained on its use. Nurses captured data about
presumptive TB patients using this tool. This application is bi-directionally connected with the NTP’s
electronic recording and reporting system, the Vietnam TB Information Management Electronic System
(VITIMES), which enabled the electronic referral of case files of persons with suspected or diagnosed
TB to NTP facilities.
Trop. Med. Infect. Dis. 2020, 5, 26 5 of 13

2.3. Study Population

All patients aged ≥15 years attending the three outpatient departments of HIGH between 24 June,
2018 and 31 December, 2018 were included.

2.4. Data Variables and Sources

Case-level covariates were extracted from the ACIS and VITIMES systems. These included
TB symptoms, chest X-ray findings, diagnostic test results, diagnoses, treatment initiation dates,
and treatment outcomes. We used name, age, and sex to merge the two databases, but removed names
and other personal identifiers before analysis to ensure confidentiality of data.

2.5. Analysis and Statistics

Data was analyzed using Stata software (version 14.0, Statacorp, Texas, TX, USA). We have
depicted the cascade of care in the form of a flowchart with dropouts at every stage summarized as
frequencies and percentages. To calculate the proportion with presumptive TB, we chose all people
attending the three out patient departments (OPD) as the denominator, because information on who
among them were screened was not available in the records. TB treatment outcomes were categorized
into successful (cured and treatment completed) and unsuccessful (failure, lost to follow-up, died,
not evaluated) outcomes. The time delays between screening, undergoing diagnostic test and initiation
of treatment were summarized using median and interquartile range (IQR). Factors associated with ‘not
getting investigated for TB’ among presumptive TB patients were assessed using adjusted risk ratios
and 95% confidence intervals (CI) calculated using log-binomial regression. We also assessed factors
associated with TB diagnosis among patients investigated for TB using the same effect measures.

2.6. Ethics Approval

Ethics approval was obtained from the Scientific Ethics Committee of the National Lung Hospital,
Hanoi, Vietnam (approval number 954/QD-BVPTU) and the Ethics Advisory Group of the International
Union Against Tuberculosis and Lung Disease, Paris, France (approval number 22/19). Since this
was a review of existing records with no direct interaction with human participants, the need for
individual informed consent was waived by the ethics committees. Confidentiality of the patient
data was ensured by (i) providing restricted access to patient data only to the research team (ii) using
password protection to access the electronic files and (iii) removing all the personal identifiers (such as
name, address, phone number) before analysis.

3. Results
A total of 52,078 adults attended the three OPDs at HIGH during the study period. Of them,
2739 (5.3%) had either symptoms suggestive of TB or were exposed to someone with TB. Of these,
1372 (50%) were male and mean (SD) age was 49 (17) years. The profile of these patients is depicted in
Table 1. Cough was the predominant symptom present in 2240 (82%) individuals, followed by chest
pain and dyspnea in 1926 (70%), fatigue in 1521 (56%) and fever in 418 (15%). Contact with a person
with TB was reported by 34 (1%) patients.
Trop. Med. Infect. Dis. 2020, 5, 26 6 of 13

Table 1. Socio-demographic and clinical profile of people with tuberculosis (TB) symptoms or contact
history attending the Haiphong International General Hospital in Vietnam, from June to December 2018.

Characteristic Number (%)

Total 2739 (100.0)
Age group (years)
15-44 1170 (42.7)
45-64 1084 (39.6)
≥ 65 485 (17.7)
Gender
Male 1372 (50.1)
Female 1367 (49.9)
Self-reported HIV status
Negative 596 (21.8)
Positive 4 (0.1)
Unknown 2139 (78.1)
Self-reported diabetes
No 1699 (62.0)
Yes 161 (5.9)
Unknown 879 (32.1)
Presenting symptoms
Cough (any duration) * 2240 (81.8)
Chest pain and dyspnea 1926 (70.3)
Fever 418 (15.3)
Fatigue 1521 (55.5)
Sweating at night 51 (1.9)
Unexplained weight loss 133 (4.9)
History of contact of TB 34 (1.2)
HIV = Human immunodeficiency virus infection, TB = Tuberculosis; * 125 of these patients had hemoptysis.

3.1. Cascade of Care

The cascade of care among study participants is depicted in Figure 1. Of the 2739 symptomatic
individuals or those with contact history, 368 (13.4%) had chest X-ray suggestive of TB and were
identified as having presumptive TB (i.e., 368/52,078 [0.7%]). Of these, 299 (81%) underwent at least one
of the diagnostic tests for TB and 103 (34.4%) were diagnosed with TB. In addition, 195/2371 (8%) patients
with normal chest X-ray also underwent tests for TB, of whom 7 (4%) cases were diagnosed. In total, 110
people were diagnosed with TB. Of the 110 TB patients, 92 (84%) had bacteriologically confirmed TB and
the rest were either clinically diagnosed or based on the results of other histopathological investigations.
Of them, 104 (95%) were initiated on anti-TB treatment. All, except one, received treatment at an NTP
health facility. Two individuals had rifampicin-resistant TB and were referred to the Provincial Lung
Hospital and subsequently treated with second-line drugs. The majority of patients had pulmonary
TB (n = 98, 88%), while the remaining 12 patients had extra-pulmonary TB (09 pleural TB and 3 lymph
node TB).
 Trop. Med.
Trop. Med.Infect.
Infect.Dis.
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FOR PEER REVIEW 7 7ofof14
13

Number of patients attending OPD

n=52,078

Presence of TB symptoms or individuals with contact history

n= 2739 (5.3%)

Chest X-Ray suggestive of TB Chest X-Ray not suggestive of TB

n=368 (13.4%) n=2371 (86.6%)

Undergone any test for TB Undergone any test for TB

n=299 (81.2%) n=195 (8.2%)

[Smear—257; Xpert—49; Culture—122; [Smear—174; Xpert—5; Culture—14;

TRC—127] TRC—26]

Results of diagnostic test Results of diagnostic test

Smear positive—46/257 (18%) Smear positive—1/174 (<1%)
Xpert positive—23/49 (47%) Xpert positive—1/5 (20%)
Culture positive—32/122 (26%) Culture positive—2/14 (14%)
TRC positive—29/127 (23%) TRC positive—1/26 (4%)

Diagnosed with TB n= 103 (34.4%) Diagnosed with TB n= 7 (3.6%)

[Bacteriologically confirmed TB = 88* [Bacteriologically confirmed TB = 4

Non bacteriologically confirmed TB = 15] Non bacteriologically confirmed TB = 3]

Initiation of TB treatment Initiation of TB treatment

n= 99 (96.1%) n= 5 (71.4%)

a Successful outcome = 92 (92.9%) Successful outcome = 5 (100%)

b Unsuccessful outcome = 5 (5.1%)

On treatment = 2 (2.0%)

Figure 1. Cascade of tuberculosis care (from screening to treatment outcome) among the patients
Figure 1. Cascade
attending of tuberculosis
the Haiphong care (from
International Generalscreening
Hospitaltointreatment
Vietnam,outcome)
from Juneamong the patients
to December 2018.
OPD = Outpatient Department; TB = tuberculosis; TRC = transcription concerted reaction. a: successful
attending the Haiphong International General Hospital in Vietnam, from June to December 2018.
OPD = Outpatient
outcome: cured andDepartment; TB = tuberculosis;
treatment completed. TRCoutcome:
B: unsuccessful = transcription concerted
death, loss reaction.
to follow-up, a:
failure,
successful outcome:*Two
and not evaluated. cured and treatment
individuals completed.
had rifampicin B: unsuccessful
resistance outcome:
and were started death, loss
on second-line to
drugs.
follow-up, failure, and not evaluated. *Two individuals had rifampicin resistance and were started
on second-line drugs.
Trop. Med. Infect. Dis. 2020, 5, 26 8 of 13

3.2. Factors Associated with ‘Not Getting Tested for TB’

Of the 368 individuals with presumptive TB, 69 (19%) did not undergo any diagnostic testing.
Patients without cough, without fever, without night sweats, without weight loss, and without TB
contact history were less likely to be tested for TB (Table 2).

Table 2. Factors associated with ‘not getting tested for TB’ among presumptive TB patients attending
the Haiphong International General Hospital in Vietnam, from June to December 2018.

Not Tested for TB# RR (95%CI) aRR (95%CI)

Characteristic Total
n (%)
Total 368 69 (18.7) - -
Age (years)
15–44 138 27 (19.6) 0.89 (0.52–1.51) 1.06 (0.97–1.08)
45–64 148 24 (16.2) 0.74 (0.43–1.28) 1.01 (0.96–1.07)
65 and above 82 18 (21.9) 1 1
Gender
Male 203 30 (14.8) 1 1
Female 165 39 (23.6) 1.60 (1.04–2.46) 1.02 (0.99–1.06)
Self-reported HIV status
Negative 195 24 (12.3) - -
Positive 1 0 (0.0) - -
Unknown 172 45 (25.2) - -
Self-reported diabetes
No 280 49 (17.5) 0.72 (0.39–1.34) 1.03 (0.94–1.13)
Yes 37 9 (24.3) 1 1
Unknown 51 11 (21.6) 0.89 (0.41–1.92) 1.17 (1.06–1.28)
Cough
No 68 20 (29.4) 1.80 (1.15–2.82) 1.07 (1.02–1.28)
Present 300 49 (16.3) 1 1
Fever
No 267 59 (22.1) 2.23 (1.19–4.19) 1.20 (1.12–1.29)
Present 101 10 (9.9) 1 1
Chest pain and dyspnea
No 128 23 (18.0) 0.94 (0.60–1.47) 0.99 (0.96–1.04)
Present 240 46 (19.2) 1 1
Fatigue
No 159 38 (23.9) 1.61 (1.05–2.47) 0.95 (0.91–0.98)
Present 209 31 (14.8) 1 1
Night sweat
No 343 68 (19.8) 4.96 (0.72–34.21) 1.37 (1.08–1.77)
Present 25 1 (4.0) 1 1
Weight loss *
No 311 65 (20.9) 2.93 (1.11–7.71) 1.38 (1.20–1.62)
Present 56 4 (7.1) 1 1
Contact history of TB
No 355 67 (18.8) 1.23 (0.34–4.47) 1.31 (1.01–1.71)
Present 13 2 (15.4) 1 1
* Data missing for one; HIV = human immunodeficiency virus; TB = tuberculosis; CI = confidence interval; aRR =
adjusted relative risk.

3.3. Factors Associated with TB Diagnosis

Of the 494 patients who underwent diagnostic tests, 110 (22%) were diagnosed with TB.
Patients with self-reported diabetes and those with weight loss had a significantly higher chance of
getting diagnosed with TB (Table 3).
Trop. Med. Infect. Dis. 2020, 5, 26 9 of 13

Table 3. Factors associated with diagnosis of TB among the patients who were investigated in the
Haiphong International General Hospital in Vietnam, from June to December 2018.

Number Confirmed TB#

Characteristic RR (95%CI) aRR (95%CI)
Tested n (%)
Total 494 110 (22.3) - -
Age (years)
15–44 191 45 (23.6) 1.32 (0.81–2.16) 1.59 (0.93–2.72)
45–64 202 47 (23.3) 1.31 (0.80–2.13) 1.33 (0.80–2.21)
65 and above 101 18 (17.8) 1 1
Gender
Male 267 63 (23.6) 1.14 (0.82–1.59) 1.01 (0.73–1.39)
Female 227 47 (20.7) 1 1
Self-reported HIV status
Negative 218 70 (32.1) - -
Positive 2 0 (0.0) - -
Unknown 274 40 (14.6) - -
Self-reported diabetes
No 375 83 (22.1) 1 1
Yes 40 16 (40.0) 1.81 (1.18–2.76) 2.13 (1.31–3.48)
Unknown 79 11 (13.9) 0.63 (0.35–1.12) 0.78 (0.44–1.39)
Cough
No 66 10 (15.1) 1 1
Present 428 100 (23.4) 1.54 (0.85–2.80) 1.42 (0.82–2.46)
Fever
No 355 69 (19.4) 1 1
Present 139 41 (29.5) 1.52 (1.08–2.13) 1.32 (0.95–1.83)
Chest pain and dyspnea
No 162 44 (27.2) 1 1
Present 332 66 (19.9) 0.73 (0.53–1.02) 0.78 (0.56–1.08)
Fatigue
No 224 40 (17.9) 1 1
Present 270 70 (25.9) 1.45 (1.03–2.05) 1.18 (0.82–1.69)
Night sweat
No 469 100 (21.3) 1 1
Present 25 10 (40.0) 1.88 (1.12–3.13) 1.31 (0.76–2.25)
Weight loss *
No 433 83 (19.2) 1 1
Present 60 27 (45.0) 2.35 (1.67–3.30) 2.06 (1.44–2.96)
Contact history of TB
No 480 105 (21.9) 1 1
Present 14 5 (35.7) 1.63 (0.79–3.36) 1.51 (0.75–3.04)
* Data missing for one; HIV = human immunodeficiency virus; TB = tuberculosis; CI = confidence interval; aRR =
adjusted relative risk.

3.4. Treatment Outcomes

The TB treatment outcomes are shown in Table 4. Among 104 patients initiated on treatment,
97 (93%) had successful treatment outcome, while 5 (5%) had unsuccessful outcome and 2 (2%) were
still on treatment.

Table 4. Treatment outcomes among tuberculosis patients started on treatment in Haiphong

International General Hospital in Vietnam, from June to December 2018.

Treatment Outcomes N (%)

Total 104 (100)
Cured 58 (55.8)
Treatment completed 39 (37.5)
Died 2 (1.9)
Lost to follow-up 3 (2.9)
On treatment * 2 (1.9)
* Two patients are on second-line treatment and are likely to complete by April 2020.
Trop. Med. Infect. Dis. 2020, 5, 26 10 of 13

3.5. Median Delays

The delays at different steps of the cascade are shown in Table 5. The median (IQR) duration from
visiting the HIGH to undergoing TB diagnostic test was 0 (0–1) day and from diagnosis to initiation of
treatment was 6 (1–17) days.

Table 5. Delays in the TB care cascade among the patients attending the Haiphong International
General Hospital in Vietnam, from June to December 2018.

Duration Number Eligible Number (%) with Median Days (IQR)

Valid Dates
From visiting the HIGH to 494 487 (99) 0 (0–1)
receiving the TB diagnosis test
From TB diagnosis to initiation 103 99 (93) 6 (1–17)
of treatment
TB = Tuberculosis; IQR = Interquartile Range; HIGH = Haiphong International General Hospital.

4. Discussion
This is the first report from Vietnam evaluating an innovative PPM model using an information
technology based tool for improving tuberculosis care in private health sector. While there are many
studies evaluating the specific components of the TB care cascade in the private sector, very few
have comprehensively examined all the steps of the cascade in a single study [16]. This is one such
effort. Overall, the performance of the model was excellent in plugging the gaps in TB care cascade in
the private sector and substantially better than previous PPM models implemented in Vietnam [13].
About 80% of the presumptive TB patients were investigated for TB. Nearly 95% of the cases diagnosed
were initiated on treatment, which is significantly better than previous studies from Vietnam and
Pakistan, where nearly 60% were lost to follow-up before treatment [13,17]. All the cases were notified
to NTP. More than 90% of all TB patients completed the treatment successfully, in line with the
global 90-(90)-90 targets. These results were better than those reported from India [18], Pakistan [17],
Thailand [19], and Vietnam [9,13] and were on par with outcomes reported from Myanmar [20].
In our view, the success of the model may be attributed to the following aspects. First, unlike earlier
PPM initiatives which predominantly used a ‘referral model’ for investigation of tuberculosis (wherein
presumptive TB patients were referred to an NTP facility), the new model offered TB tests on-site or
arranged for transportation of sputum samples. This might have reduced the gaps and delays in testing.
Second, the use of a mobile application enabled notification of every TB case diagnosed. This alerted
the health care system and the last-mile service providers like CHWs to proactively track and provide
follow-up care to the patients, thus reducing gaps in treatment initiation and completion. Third,
all the providers were trained and performance-based incentives were offered for every successful
event in the care cascade. The total costs incurred were modest at 4100 USD for the six-month pilot
period (equivalent to ~37 USD per TB case diagnosed). However, we have not undertaken a detailed
cost-effectiveness analysis. This should be a topic of future research.
There were some other notable findings. First, only 0.7% of patients attending the OPD were
identified as ‘presumptive TB’ patients. This is substantially lower than that reported from other
settings like Pakistan (which varied from 2.9% to 7.5%) [21,22]. This difference is likely due to many
differences between the settings which include (i) a stricter definition used for ‘presumptive TB’
(both symptom positive and chest X-ray abnormality) and (ii) the denominator being all patients
attending OPD rather than the number screened in our study. It is possible that some of the patients
attending the OPD might not have been screened and there was no documentation to find out the
exact numbers screened.
Second, about one in five presumptive TB patients did not undergo investigations and people
without symptoms were less likely to undergo investigation. This is concordant with the observations
by Creswell et al. in Karachi, Pakistan [22]. Patients without symptoms may have low risk perception or
Trop. Med. Infect. Dis. 2020, 5, 26 11 of 13

may have been accorded lower priority for testing by attending clinicians. Some patients may not have
been able to produce a sputum sample. The high costs of the diagnostic tests for which patients had to
pay out of pocket may have been another deterrent for uptake of tests. Also, people with symptoms
but normal chest X-ray were less likely to be tested. This may be again related to the definition of
presumptive TB used in this project, which required an abnormal X-ray in addition to symptoms.
This may also be the reason for the high yield of TB (33%) among people with presumptive TB.
Had we tested everyone with symptoms, we might have had lower yield in terms of percentage,
but more cases in terms of absolute numbers. Of course, this would have had additional cost
implications. One possible way to increase the number of cases detected without too much additional
effort will be to use the duration of symptoms to prioritize investigation for TB—like investigating
only those with cough of more than or equal to 2 weeks rather than testing everyone with cough of any
duration [23]. Unfortunately, we did not have information on duration of symptoms and hence we
cannot comment on this issue any further. All these call for revisiting the definition of presumptive TB
used in the project.
Third, a standard diagnostic algorithm was not followed in the project. The nature and the
number of tests offered to each patient seemed to vary. While we do not know the exact reasons for
this variation, we speculate that this was dependent on the ability of individual patients to afford
the high costs of the tests and based on the physician’s choice of diagnostic test. This aspect needs
to be studied further using qualitative research methods. We recommend that all patients undergo
a standard diagnostic algorithm, preferably using tests approved globally for use and, if possible,
at subsidized costs.
The study had some limitations. First, we relied on routinely collected data and hence errors in
documentation cannot be ruled out. However, we estimate that such errors are limited in number
and impact given real-time and post hoc data validation mechanisms in the ACIS software and by
data management team. Second, there was no documentation about the number of people screened.
As a result, we were unable to calculate the ‘number needed to screen’ to detect an additional TB case.
Also, the patients attending only three OPDs were screened. Hence the number of TB cases diagnosed
may not reflect the true burden of TB among patients attending HIGH. We may have missed many
patients, especially those with extrapulmonary TB because departments such as surgery, gynecology
and urology were not involved in the project. We may also have missed many patients because of
the strict definition of presumptive TB used in our study. In a national TB prevalence survey from
Vietnam, only 10% of all presumptive TB patients fulfilled such strict criteria and accounted for only
27% of all TB patients [24]. Third, the study was conducted in a single hospital thereby limiting its
generalizability. For this reason, we have refrained from the assessing the impact of this intervention
on case notification at the community level. This kind of impact has been demonstrated by previous
studies elsewhere [18,21,25]. Fourth, we did not have data for the pre-intervention period to enable
before–after comparisons. There was no systematic recording and reporting of TB-related indicators
before the study. The data obtained in this study may act as a baseline for any future evaluations.
Finally, the exact reasons for the gaps at each step of the cascade were not investigated in this study.
Future research should look into this aspect using qualitative research methods.
In conclusion, the new PPM model in Vietnam performed well with high levels of testing, diagnosis,
treatment start and completion among TB patients. Given the success of this model in plugging the
gaps in TB care cascade, the NTP in Vietnam is considering to scale-up this model nationwide after
undertaking a detailed cost-effectiveness analysis. The lessons learned from this study may be useful
to make amendments in the PPM model and optimize project implementation going forward.

Author Contributions: Conceptualization and protocol development: T.D.T., A.M.V.K., G.R., T.H., H.L.V.,
L.N.Q.V., H.N.T., A.C., R.F., T.T.T.D., T.H., H.N.V., H.B.V., H.N.B., and N.N.V. Data Collection: T.D.T., T.T.T.D.,
and A.C. Data Analysis or interpretation: T.D.T., A.M.V.K., G.R., T.H., and J.C. Writing the first draft: T.D.T.,
A.M.V.K., and G.R. Critical review of the paper and final approval: T.D.T., A.M.V.K., G.R., H.L.V., L.N.Q.V., H.N.T.,
A.C., R.F., T.T.T.D., H.N.V., H.B.V., H.N.B., N.N.V., and J.C. All authors have read and agreed to the published
version of the manuscript.
Trop. Med. Infect. Dis. 2020, 5, 26 12 of 13

Funding: This research study was generously supported by a grant from the Stop TB Partnership’s TB REACH
initiative, with funding from Global Affairs Canada. The training program, within which this paper was developed,
and the open access publication costs were funded by Department for International Development (DFID), UK and
La Fondation Veuve Emile Metz-Tesch (Luxembourg). The funders had no role in study design, data collection
and analysis, decision to publish, or preparation of the manuscript.
Acknowledgments: This research was conducted through the Structured Operational Research and Training
Initiative (SORT IT), a global partnership led by the Special Program for Research and Training in Tropical Diseases at
the World Health Organization (WHO/TDR). The model is based on a course developed jointly by the International
Union Against Tuberculosis and Lung Disease (The Union) and Medécins sans Frontières (MSF/Doctors Without
Borders). The specific SORT IT program which resulted in this publication was jointly developed and implemented
by: The Union South-East Asia Office, New Delhi, India; the Centre for Operational Research, The Union, Paris,
France; The Union, Mandalay, Myanmar; The Union, Harare, Zimbabwe; MSF Luxembourg Operational Research
(LuxOR); MSF Operational Center Brussels (MSF OCB); Jawaharlal Institute of Postgraduate Medical Education
and Research (JIPMER), Puducherry, India; Post Graduate Institute of Medical Education and Research (PGIMER),
Chandigarh, India; All India Institute of Medical Sciences (AIIMS), New Delhi, India; Velammal Medical College
Hospital and Research Institute, Madurai, India; Society for Education Welfare and Action (SEWA)—Rural,
Jhagadia, India; Common Management Unit (AIDS, TB & Malaria), Ministry of National Health Services,
Regulations and Coordination, Islamabad, Pakistan; and Kidu Mobile Medical Unit, His Majesty’s People’s Project
and Jigme Dorji Wangchuck National Referral Hospital, Thimphu, Bhutan. The authors would also like to thank
the Vietnam National Tuberculosis Control Programme, Friends for International Tuberculosis Relief, Ho Chi
Minh City, Vietnam, Haiphong International General Hospital for their support, the Stop TB Partnership’s TB
REACH for providing grant, and the community health workers for their help with data collection and follow-up
of TB patients.
Conflicts of Interest: The authors declare no conflict of interest.

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